Natural allelic variation confers diversity in the regulation of flag leaf traits in wheat.
Bread wheat
Candidate genes
FarmCPU
Flag leaf area
GWAS
Grain yield
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
10 06 2024
10 06 2024
Historique:
received:
08
11
2023
accepted:
05
06
2024
medline:
11
6
2024
pubmed:
11
6
2024
entrez:
10
6
2024
Statut:
epublish
Résumé
Flag leaf (FL) dimension has been reported as a key ecophysiological aspect for boosting grain yield in wheat. A worldwide winter wheat panel consisting of 261 accessions was tested to examine the phenotypical variation and identify quantitative trait nucleotides (QTNs) with candidate genes influencing FL morphology. To this end, four FL traits were evaluated during the early milk stage under two growing seasons at the Leibniz Institute of Plant Genetics and Crop Plant Research. The results showed that all leaf traits (Flag leaf length, width, area, and length/width ratio) were significantly influenced by the environments, genotypes, and environments × genotypes interactions. Then, a genome-wide association analysis was performed using 17,093 SNPs that showed 10 novel QTNs that potentially play a role in modulating FL morphology in at least two environments. Further analysis revealed 8 high-confidence candidate genes likely involved in these traits and showing high expression values from flag leaf expansion until its senescence and also during grain development. An important QTN (wsnp_RFL_Contig2177_1500201) was associated with FL width and located inside TraesCS3B02G047300 at chromosome 3B. This gene encodes a major facilitator, sugar transporter-like, and showed the highest expression values among the candidate genes reported, suggesting their positive role in controlling flag leaf and potentially being involved in photosynthetic assimilation. Our study suggests that the detection of novel marker-trait associations and the subsequent elucidation of the genetic mechanism influencing FL morphology would be of interest for improving plant architecture, light capture, and photosynthetic efficiency during grain development.
Identifiants
pubmed: 38858489
doi: 10.1038/s41598-024-64161-x
pii: 10.1038/s41598-024-64161-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
13316Subventions
Organisme : Deutsche Forschungsgemeinschaft
ID : 491250510
Informations de copyright
© 2024. The Author(s).
Références
Grote, U., Fasse, A., Nguyen, T. T. & Erenstein, O. Food security and the dynamics of wheat and maize value chains in Africa and Asia. Front. Sustain. Food Syst. 4, 617009 (2021).
doi: 10.3389/fsufs.2020.617009
Poutanen, K. S. et al. Grains–a major source of sustainable protein for health. Nutr. Rev. 80(6), 1648–1663 (2022).
pubmed: 34741520
pmcid: 9086769
doi: 10.1093/nutrit/nuab084
Yan, X. et al. QTL mapping for flag leaf-related traits and genetic effect of QFLW-6A on flag leaf width using two related introgression line populations in wheat. PLoS ONE 15(3), e0229912 (2020).
pubmed: 32191715
pmcid: 7082017
doi: 10.1371/journal.pone.0229912
Hall, A. J. & Richards, R. A. Prognosis for genetic improvement of yield potential and water-limited yield of major grain crops. Field Crop Res. 143, 18–33 (2013).
doi: 10.1016/j.fcr.2012.05.014
Duncan, W. G. Leaf angles, leaf area, and canopy photosynthesis 1. Crop Sci. 11(4), 482–485 (1971).
doi: 10.2135/cropsci1971.0011183X001100040006x
Simón, M. R. Inheritance of flag-leaf angle, flag-leaf area and flag-leaf area duration in four wheat crosses. Theor. Appl. Genet. 98(2), 310–314 (1999).
doi: 10.1007/s001220051074
Sharma, S. N., Sain, R. S. & Sharma, R. K. The genetic control of flag leaf length in normal and late sown durum wheat. J. Agric. Sci. 141(3–4), 323–331 (2003).
doi: 10.1017/S0021859603003642
Maydup, M. L., Antonietta, M., Graciano, C., Guiamet, J. J. & Tambussi, E. A. The contribution of the awns of bread wheat (Triticum aestivum L.) to grain filling: Responses to water deficit and the effects of awns on ear temperature and hydraulic conductance. Field Crops Res. 167, 102–111 (2014).
doi: 10.1016/j.fcr.2014.07.012
Siddiqui, M. N. et al. New drought-adaptive loci underlying candidate genes on wheat chromosome 4B with improved photosynthesis and yield responses. Physiol. Plantarum 173(4), 2166–2180 (2021).
doi: 10.1111/ppl.13566
Muhammad, A. et al. Uncovering genomic regions controlling plant architectural traits in hexaploid wheat using different GWAS models. Sci. Rep. 11(1), 1–14 (2021).
doi: 10.1038/s41598-021-86127-z
Gooding, M. J., Dimmock, J. P. R. E., France, J. & Jones, S. A. Green leaf area decline of wheat flag leaves the influence of fungicides and relationships with mean grain weight and grain yield. Ann. Appl. Biol. 136(1), 77–84 (2000).
doi: 10.1111/j.1744-7348.2000.tb00011.x
Schierenbeck, M., Fleitas, M. C., Gerard, G. S., Dietz, J. I. & Simón, M. R. Combinations of fungicide molecules and nitrogen fertilization revert nitrogen yield reductions generated by Pyrenophora tritici-repentis infections in bread wheat. Crop Protect. 121, 173–181 (2019).
doi: 10.1016/j.cropro.2019.04.004
Blandino, M. & Reyneri, A. Effect of fungicide and foliar fertilizer application to winter wheat at anthesis on flag leaf senescence, grain yield, flour bread-making quality and DON contamination. Eur. J. Agron. 30(4), 275–282 (2009).
doi: 10.1016/j.eja.2008.12.005
Schierenbeck, M., Fleitas, M. C., Miralles, D. J. & Simón, M. R. Does radiation interception or radiation use efficiency limit the growth of wheat inoculated with tan spot or leaf rust?. Field Crops Res. 199, 65–76 (2016).
doi: 10.1016/j.fcr.2016.09.017
Fan, X. et al. QTLs for flag leaf size and their influence on yield-related traits in wheat (Triticum aestivum L.). Mol. Breeding. 35(1), 1–16 (2015).
doi: 10.1007/s11032-015-0205-9
Ma, J. et al. Flag leaf size and posture of bread wheat: Genetic dissection, QTL validation and their relationships with yield-related traits. Theor. Appl. Genet. 133(1), 297–315 (2020).
pubmed: 31628527
doi: 10.1007/s00122-019-03458-2
Chen, S., Liu, F., Wu, W., Jiang, Y. & Zhan, K. An SNP-based GWAS and functional haplotype-based GWAS of flag leaf-related traits and their influence on the yield of bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 134(12), 3895–3909 (2021).
pubmed: 34436627
doi: 10.1007/s00122-021-03935-7
Li, H. F., Wang, J. T., Zhao, Q., & Zhang, Y. M. BLUPmrMLM: A fast mrMLM algorithm in genome-wide association studies. Genom. Proteom. Bioinform. qzae020 (2024).
Yang, D. et al. Genetic dissection of flag leaf morphology in wheat (Triticum aestivum L.) under diverse water regimes. BMC Genet. 17(1), 1–15 (2016).
pubmed: 26866367
pmcid: 4895282
doi: 10.1186/s12863-016-0399-9
Tu, Y. et al. QTL mapping and validation of bread wheat flag leaf morphology across multiple environments in different genetic backgrounds. Theor. Appl. Genet. 134(1), 261–278 (2021).
pubmed: 33026461
doi: 10.1007/s00122-020-03695-w
Wang, Y. et al. Identification of genetic loci for flag-leaf-related traits in wheat (Triticum aestivum L.) and their effects on grain yield. Front. Plant Sci. 13, 990287–990287 (2022).
pubmed: 36160981
pmcid: 9493265
doi: 10.3389/fpls.2022.990287
Kong, B. et al. Deciphering key genomic regions controlling flag leaf size in wheat via integration of meta-QTL and in silico transcriptome assessment. BMC Genom. 24(1), 1–17 (2023).
doi: 10.1186/s12864-023-09119-5
Alqudah, A. M. & Schnurbusch, T. Barley leaf area and leaf growth rates are maximized during the pre-anthesis phase. Agronomy 5(2), 107–129 (2015).
doi: 10.3390/agronomy5020107
Alqudah, A. M., Youssef, H. M., Graner, A. & Schnurbusch, T. Natural variation and genetic make-up of leaf blade area in spring barley. Theor. Appl. Genet. 131(4), 873–886 (2018).
pubmed: 29350248
pmcid: 5852197
doi: 10.1007/s00122-018-3053-2
Ding, X., Li, X. & Xiong, L. Evaluation of near-isogenic lines for drought resistance QTL and fine mapping of a locus affecting flag leaf width, spikelet number, and root volume in rice. Theor. Appl. Genet. 123(5), 815–826 (2011).
pubmed: 21681490
doi: 10.1007/s00122-011-1629-1
Wang, P., Zhou, G., Cui, K., Li, Z. & Yu, S. Clustered QTL for source leaf size and yield traits in rice (Oryza sativa L.). Mol. Breeding 29, 99–113 (2012).
doi: 10.1007/s11032-010-9529-7
Zhao, C. et al. Fine mapping of QFlw-5B, a major QTL for flag leaf width in common wheat (Triticum aestivum L.). Theor. Appl. Genet. 135(7), 2531–2541 (2022).
pubmed: 35680741
doi: 10.1007/s00122-022-04135-7
Wu, Q. et al. QTL mapping of flag leaf traits in common wheat using an integrated high-density SSR and SNP genetic linkage map. Euphytica 208, 337–351 (2016).
doi: 10.1007/s10681-015-1603-0
Liu, G. et al. Mapping QTLs of yield-related traits using RIL population derived from common wheat and Tibetan semi-wild wheat. Theor. Appl. Genet. 127, 2415–2432 (2014).
pubmed: 25208643
doi: 10.1007/s00122-014-2387-7
Yan, X. et al. Identification of genetic loci and a candidate gene related to flag leaf traits in common wheat by genome-wide association study and linkage mapping. Mol. Breeding 40, 58. https://doi.org/10.1007/s11032-020-01135-7 (2020).
doi: 10.1007/s11032-020-01135-7
Xue, S. et al. Fine mapping TaFLW1, a major QTL controlling flag leaf width in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 126(8), 1941–1949 (2013).
pubmed: 23661078
doi: 10.1007/s00122-013-2108-7
Berthet, S. et al. Role of plant laccases in lignin polymerization. in Advances in Botanical Research (Vol. 61, pp. 145–172). (Academic Press, 2012).
Schierenbeck, M. et al. Genetic dissection of grain architecture-related traits in a winter wheat population. BMC Plant Biol. 21(1), 1–14 (2021).
Schierenbeck, M. et al. Association mapping unravels the genetics controlling seedling drought stress tolerance in winter wheat. Front. Plant Sci. 14, 1061845. https://doi.org/10.3389/fpls.2023.1061845 (2023).
doi: 10.3389/fpls.2023.1061845
pubmed: 36818842
pmcid: 9933780
Zadoks, J. C., Chang, T. T. & Konzak, C. F. A decimal code for the growth stages of cereals. Weed Res. 14(6), 415–421 (1974).
doi: 10.1111/j.1365-3180.1974.tb01084.x
Liu, K. et al. QTL mapping of flag leaf-related traits in wheat (Triticum aestivum L.). Theor. Appl. Genet. 131(4), 839–849 (2018).
pubmed: 29359263
pmcid: 5852184
doi: 10.1007/s00122-017-3040-z
Goedhart, P.W. Procedure VSEARCH. in Biometrics. GenStat Procedure Library Manual 18th Edition. (Wageningen University, 2016)
VSN International. Genstat for Windows 18th edn. (VSN International Ltd., 2015).
Falconer, D.S., & T.F. Mackay. Introduction to Quantitative Genetics (Pearson Prentice Hall, 2005). Fourth.
Julkowska, M. M. et al. MVApp—Multivariate analysis application for streamlined data analysis and curation. Plant Physiol. 180(3), 1261–1276 (2019).
pubmed: 31061104
pmcid: 6752927
doi: 10.1104/pp.19.00235
Pinheiro, J., Bates, D., R Core Team. Nlme: Linear and nonlinear mixed effects models. R package version 3.1-159 (2022).
Wang, S. et al. Characterization of polyploid wheat genomic diversity using a high-density 90,000 single nucleotide polymorphism array. Plant Biotechnol. J. 12(6), 787–796 (2014).
pubmed: 24646323
pmcid: 4265271
doi: 10.1111/pbi.12183
Wang, J. & Zhang, Z. GAPIT version 3: Boosting power and accuracy for genomic association and prediction. Genom. Proteom. Bioinform. 19(4), 629–640 (2021).
doi: 10.1016/j.gpb.2021.08.005
Liu, X., Huang, M., Fan, B., Buckler, E. S. & Zhang, Z. Iterative usage of fixed and random effect models for powerful and efficient genome-wide association studies. PLoS Genet. 12(2), e1005767 (2016).
pubmed: 26828793
pmcid: 4734661
doi: 10.1371/journal.pgen.1005767
Alqudah, A. M., Sallam, A., Baenziger, P. S. & Börner, A. GWAS: Fast-forwarding gene identification and characterization in temperate cereals: lessons from barley—A review. J. Adv. Res. 22, 119–135 (2020).
pubmed: 31956447
doi: 10.1016/j.jare.2019.10.013
Quan, X. et al. Genome-wide association study uncover the genetic architecture of salt tolerance-related traits in common wheat (Triticum aestivum L.). Front. Genet. 12, 663941 (2021).
pubmed: 34093656
pmcid: 8172982
doi: 10.3389/fgene.2021.663941
Ramírez-González, R. H. et al. The transcriptional landscape of polyploid wheat. Science 361(6403), eaar6089 (2018).
pubmed: 30115782
doi: 10.1126/science.aar6089
Alemu, A. et al. Genome-wide association analysis and genomic prediction for adult-plant resistance to Septoria tritici blotch and powdery mildew in winter wheat. Front. Genet. 12, 661742 (2021).
pubmed: 34054924
pmcid: 8149967
doi: 10.3389/fgene.2021.661742
Muellner, A. E. et al. Comparative mapping and validation of multiple disease resistance QTL for simultaneously controlling common and dwarf bunt in bread wheat. Theor. Appl. Genet. 134, 489–503 (2021).
pubmed: 33120433
doi: 10.1007/s00122-020-03708-8
Sun, Z. et al. tRNA-derived fragments from wheat are potentially involved in susceptibility to Fusarium head blight. BMC Plant Biol. 22(1), 1–17 (2022).
doi: 10.1186/s12870-021-03393-9
Rahman, M. Improving the crown rot resistance and tolerance of wheat using marker-assisted recurrent selection (Doctoral dissertation, 328 Pages, 2018). https://ses.library.usyd.edu.au/bitstream/handle/2123/19643/Rahman_Mahbubur_Thesis_440577148.pdf?sequence=2
Zheng, W., Shi, Z., Long, M. & Liao, Y. Quantitative proteomics analysis identifies the potential mechanism underlying yellow-green leave mutant in wheat. Phyton 90(4), 1147 (2021).
doi: 10.32604/phyton.2021.015916
Naraghi, S. M. et al. Deciphering the genetics of major end-use quality traits in wheat. G3 Genes Genomes Genet. 9(5), 1405–1427 (2019).
doi: 10.1534/g3.119.400050
Iannucci, A., et al. Mapping QTL for root and shoot morphological traits in a durum wheat × T. dicoccum segregating population at seedling stage. Int. J. Genom. 2017 (2017).
Maccaferri, M. et al. Prioritizing quantitative trait loci for root system architecture in tetraploid wheat. J. Exp. Bot. 67(4), 1161–1178 (2016).
pubmed: 26880749
pmcid: 4753857
doi: 10.1093/jxb/erw039
Amo, A. & Soriano, J. M. Unravelling consensus genomic regions conferring leaf rust resistance in wheat via meta-QTL analysis. Plant Genome 15(1), e20185 (2022).
pubmed: 34918873
doi: 10.1002/tpg2.20185
Saini, D. K., Srivastava, P., Pal, N. & Gupta, P. K. Meta-QTLs, ortho-meta-QTLs and candidate genes for grain yield and associated traits in wheat (Triticum aestivum L.). Theor. Appl. Genet. 135(3), 1049–1081 (2022).
pubmed: 34985537
doi: 10.1007/s00122-021-04018-3
Lou, H. et al. Genome-wide association study of six quality-related traits in common wheat (Triticum aestivum L.) under two sowing conditions. Theor. Appl. Genet. 134, 399–418 (2021).
pubmed: 33155062
doi: 10.1007/s00122-020-03704-y
Kartseva, T. et al. Nutritional genomic approach for improving grain protein content in wheat. Foods 12(7), 1399 (2023).
pubmed: 37048220
pmcid: 10093644
doi: 10.3390/foods12071399
Zou, J. et al. QTLs associated with agronomic traits in the Attila× CDC Go spring wheat population evaluated under conventional management. PloS One 12(2), e0171528 (2017).
pubmed: 28158253
pmcid: 5291526
doi: 10.1371/journal.pone.0171528
Amalova, A., Abugalieva, S., Babkenov, A., Babkenova, S. & Turuspekov, Y. Genome-wide association study of yield components in spring wheat collection harvested under two water regimes in Northern Kazakhstan. PeerJ 9, e11857 (2021).
pubmed: 34395089
pmcid: 8323601
doi: 10.7717/peerj.11857
Sheoran, S. et al. Genome-wide association study and post-genome-wide association study analysis for spike fertility and yield related traits in bread wheat. Front. Plant Sci. 12, 3452 (2022).
doi: 10.3389/fpls.2021.820761
Genievskaya, Y., Turuspekov, Y., Rsaliyev, A. & Abugalieva, S. Genome-wide association mapping for resistance to leaf, stem, and yellow rusts of common wheat under field conditions of South Kazakhstan. PeerJ 8, e9820 (2020).
pubmed: 32944423
pmcid: 7469934
doi: 10.7717/peerj.9820
Szeliga, M., Bakera, B., Święcicka, M., Tyrka, M. & Rakoczy-Trojanowska, M. Identification of candidate genes responsible for chasmogamy in wheat. BMC Genom. 24(1), 170 (2023).
doi: 10.1186/s12864-023-09252-1
Du, B. et al. Genome-wide meta-analysis of QTL for morphological related traits of flag leaf in bread wheat. Plos One 17(10), e0276602 (2022).
pubmed: 36279291
pmcid: 9591062
doi: 10.1371/journal.pone.0276602
Shariatipour, N., Heidari, B., Tahmasebi, A. & Richards, C. Comparative genomic analysis of quantitative trait loci associated with micronutrient contents, grain quality, and agronomic traits in wheat (Triticum aestivum L.). Front. Plant Sci. 12, 709817 (2021).
pubmed: 34712248
pmcid: 8546302
doi: 10.3389/fpls.2021.709817
Rolland, F., Baena-Gonzalez, E. & Sheen, J. Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu. Rev. Plant Biol. 57, 675–709 (2006).
pubmed: 16669778
doi: 10.1146/annurev.arplant.57.032905.105441
Paulsen, P. A., Custódio, T. F. & Pedersen, B. P. Crystal structure of the plant symporter STP10 illuminates sugar uptake mechanism in monosaccharide transporter superfamily. Nat. Commun. 10, 407 (2019).
pubmed: 30679446
pmcid: 6345825
doi: 10.1038/s41467-018-08176-9
Schofield, R. A., Bi, Y. M., Kant, S. & Rothstein, S. J. Over-expression of STP13, a hexose transporter, improves plant growth and nitrogen use in Arabidopsis thaliana seedlings. Plant Cell Environ. 32, 271–285 (2009).
pubmed: 19054349
doi: 10.1111/j.1365-3040.2008.01919.x
Rottmann, T. et al. Sugar transporter STP7 specificity for l-arabinose and d-xylose contrasts with the typical hexose transporters STP8 and STP12. Plant Physiol. 176, 2330–2350 (2018).
pubmed: 29311272
pmcid: 5841717
doi: 10.1104/pp.17.01493
Huai, B. et al. ABA-induced sugar transporter TaSTP6 promotes wheat susceptibility to stripe rust. Plant Physiol. 181, 1328–1343 (2019).
pubmed: 31540949
pmcid: 6836835
doi: 10.1104/pp.19.00632
Lemonnier, P. et al. Expression of Arabidopsis sugar transport protein STP13 differentially affects glucose transport activity and basal resistance to Botrytis cinerea. 85, 473–484 (2014).
Vargas, W. A. et al. Plant defense mechanisms are activated during biotrophic and necrotrophic development of Colletotricum graminicola in maize. Plant Physiol. 158(3), 1342–1358 (2012).
pubmed: 22247271
pmcid: 3291271
doi: 10.1104/pp.111.190397
Wang, G. et al. TaSYP137 and TaVAMP723, the SNAREs proteins from wheat, reduce resistance to Blumeria graminis f. sp. tritici. Int. J. Mol. Sci. 24(5), 4830 (2023).
pubmed: 36902258
pmcid: 10003616
doi: 10.3390/ijms24054830
Zapata, J. M., Martínez-García, V. & Lefebvre, S. Phylogeny of the TRAF/MATH domain. TNF receptor associated factors (TRAFs). Adv. Exp. Med. Biol. 597, 1–24 (2007).
pubmed: 17633013
doi: 10.1007/978-0-387-70630-6_1
Ao, K. et al. Puncta-localized TRAF domain protein TC1b contributes to the autoimmunity of snc1. Plant J. 114, 591–612 (2023).
pubmed: 36799433
doi: 10.1111/tpj.16155